Loss of Vertically-Inherited Totiviruses and Toxin-Encoding Satellites in Killer Yeast Evidences Intracellular Conflict in Natural Populations

Saccharomyces cerevisiae is occasionally infected by totiviruses and their toxin-encoding satellites. Totiviruses and their satellites coexist but with an asymmetric dependence on the totivirus for maintenance inside the host cell. Satellites provide their yeast hosts with inhibitory toxins and the necessary self-immunity; loss of the satellite equates to loss of immunity. Because mycoviruses lack known extracellular stages, and sex is considered rare, mycoviruses are assumed to be transmitted vertically, implying infection states should correlate with host genotypes. However, totivirus-satellite coinfections are rarely examined in natural populations, leaving their associations with host genotypes poorly understood. We screened a multiyear population of S. cerevisiae isolates from New Zealand to examine the stability of host-virus associations over time, both within and across genotypes. While 55% of wild isolates harbored infections, only 37% of these included toxin-encoding satellites. Genotypes that persisted across years typically maintained consistent infection states. However, we observed stepwise transitions including acquisitions of totiviruses and satellites. Genotypes clustered strongly by infection state, supporting vertical transmission while suggesting that outcrossing is not responsible for the mycovirus acquisitions. Despite infection changes, genotype clustering by infection state remained intact, suggesting transitions are transient and that host genotypes may have optimal totivirus-satellite infection states.